- Email: [email protected]
Evaluation of normal and abnormal hyoid bone movement during swallowing by use of ultrasound duplex-Doppler imaging
in Med. & Bml., Vol. 22. No. 9. pp. 1169- 1175, 1996 0 1996 World Federation for Ultrasound in Medicine & Biology Printed in the USA. All rights reserved 0301.5629/96 $15.00 + .JO
Ultrasound
Copyright
PII: SO301-5629( 96)00158-S
ELSEVIER
l
Original Contribution EVALUATION OF NORMAL AND ABNORMAL HYOID BONE MOVEMENT DURING SWALLOWING BY USE OF ULTRASOUND DUPLEX-DOPPLER IMAGING BARBARA C. SONIES,+ CHENG WANG* and DARREN J. SAPPER’ +Rehabilitation Medicine Department, National Institutes of Health, Bethesda, MD: and ‘Allied Imaging International, Inc., Germantown, MD (Received
20 Fehruqv
1996; in finulforttz
I Augusf
1996)
Abstract-We developed a new method to analyze normal and abnormal movements of the hyoid muscular region as an indicator of hyoid bone motion during swallowing using ultrasound duplex-Doppler imaging. Hyoid bone motion can be monitored by studying the Doppler shift spectra and B-mode images produced by ultrasound duplex imaging of the hyoid region muscular attachments. We can accurately determine swallowing duration and trajectory of hyoid bone movement. This procedure can assist in discriminating between normal and abnormal movements of the hyoid bone and the surrounding muscles during swallowing. This method appears to be a highly consistent measure. We suggest that Doppler spectrum analysis can be used for defining hyoid position and displaying accurate movement, which may he useful in the Copyright 0 1996 World Federation for Ultrasound in Medicine & Biology diagnosis of swallowing disorders. Key Words: Ultrasound
imaging, Ultrasound
duplex-Doppler
INTRODUCTION
radiology. Being able to provide real-time images, ultrasound imaging techniques have been used in speech and swallowing studies (Cordaro and Sonies 1993; Shawker et al. 1983, 1984a; Sonies et al. 1981, 1988) and in the study of soft tissue anatomy of the tongue and floor of the mouth (Shawker et al. 1984b). Although ultrasound cannot display the hyoid bone itself, conventional Bmode scanning can still be used to monitor hyoid bone movement by analyzing the motion of its acoustic shadow and the surrounding muscle tissues (i.e., the hyomuscular attachment region) (Brown and Sonies 1996; Sonies and Stone 1996). The ultrasonic duplex-Doppler imaging technique, which provides both echographic B-mode images and Doppler shift spectra, is frequently used to analyze motion of blood flow through the cardiovascular system. Davidson (1988) used Doppler methods along with other velocimetric techniques to study the temporomandibular joint (TMJ) Marini et al. ( 1994) reported a novel approach to evaluate the pathophysiology of the TMJ by using ultrasound duplex-Doppler spectral analysis techniques. In their study, joint movement was analyzed by computing the Fourier transform of the time signals. which gave the velocity distribution of the condylo-mensical complex during opening and closing of the jaw. They were able to discriminate
The larynx and pharynx are muscular tubes surrounded by a suspensory system composed of the hyoid bone and the thyroid and cricoid cartilages, which are all interlinked by ligaments and tendons. These structures maintain the lumen of the pharynx and larynx. The whole complex is attached to the base of the skull, mandible, spine and thoracic skeleton. The supra- and infrahyoid muscles (mylohyoid, geniohyoid, digastic, stylohyoid) all attach to the hyoid bone beneath the chin in a submental position. This area can be called the hyomuscular region (HMR). The hyoid bone, which has a characteristic radiographic appearance, is a critical component of this system. The movement of the hyoid bone is thought to be important for closure of the airway, including the lowering of the epiglottis and the adduction of the vocal folds. Movement of the hyoid bone is traditionally studied using x-ray fluoroscopy, which exposes subjects to radiation (Dodds et al. 1988; Ekberg 1986; Wintzen et al. 1994). However, as a noninvasive technology, ultrasound imaging is playing a growing role in diagnostic Address correspondence Speech-Language Pathology partment, National Institutes
imaging, Hyoid bone motion, Swallowing.
to: Dr. Barbara C. Sonies, Chief. Section, Rehabilitation Medicine Deof Health, Bethesda, MD 20892. 1169
1170
Ultrasound in Medicine and Biology
between normal and abnormal motions of the condylomensical complex. We propose the use of ultrasound duplex-Doppler imaging for the assessment of hyoid bone motion during swallowing. To investigate the feasibility of using ultrasound duplex-Doppler imaging for assessing the movement of the hyoid bone during swallowing, we have developed a computerized image acquisition and processing system that allows us to acquire B-mode ultrasound images and analyze Doppler spectra data. Using our technique, we studied controlled water bolus swallows of normal subjects and patients with swallowing disorders. We compared swallow duration, hyoid bone movement trajectories and hyoid bone velocities based upon the displacement of the HMR to evaluate swallowing. We describe the image acquisition and processing system and the results of the analysis of normal and abnormal hyoid bone movement. MATERIALS
AND METHODS
An ATL Ultramark 9 HDI ultrasound scanner (Advanced Technology Laboratories, Inc., Bothell, WA, USA) was used for the studies. Images were acquired using a curved array transducer with an operating frequency range from 5.0-9.0 MHz and a Doppler frequency of 5.0 MHz. Figure 1 shows a configuration diagram of our ultrasound duplex-Doppler
n $ Subject
Ultrasound Transducer
ATL Ultramark 9 Ultrasound Imaging
Volume 22, Number 9, 1996
image acquisition system. To obtain images, the transducer was placed submentally under the subject’s chin and angled back toward the hyoid bone shadow, with the hyomuscular attachment region in clear view. The position and orientation of the transducer and the position of the sampling volume were adjusted by viewing the two-dimensional (2D) echographic images. The images containing both the 2D images and Doppler spectra were recorded on video tape for analysis. A time code indicating the video frame was inserted on the images (Horita TRG-50, Horita, Mission Viejo, CA, USA). The image data on the tape were digitized using a frame grabber board (Scion LG-3, Scion Corporation, Frederick, MD, USA) on a Macintosh Quadra 700 computer (Apple Computer, Inc., Santa Clara, CA, USA). Two dimensional B-mode echographic images were displayed simultaneously with Doppler spectral signals. Simultaneous display was needed to adjust the size and position of the Doppler sampling volume as well as to adjust the angle between the ultrasound beam and the hyoid bone. The hyomuscular attachment region, where all the muscles attach to the superior cornu of the hyoid bone, creates a highly echoic region in the image. The sample volume is positioned over this readily visible region. The acoustic shadow of the hyoid is an echo-free triangular area adjacent to the HMR through which the Doppler beam passes (Fig. 2). Figure 2 shows a standard mid-line sagittal ultrasound Doppler image through the tongue and oral cavity, with the central axis of the Doppler beam and fixed sampling volume indicated. On the B-mode image, the Doppler beam was oriented through the HMR, which could be seen as a bright area (boxed in) at the origin of the acoustic shadow cast by the hyoid bone. Because ultrasound does not image bone, this technique relies upon measuring the displacement motion through the fixed sample volume of the HMR. The ATL Doppler equipment is designed to display the beam’s central axis and selected sample volume. The initial motion of the HMR away from the transducer produces a Doppler frequency shift. The Doppler frequency shift depends on the velocity, u, of the observed object (i.e. , the hyoid bone and its surrounding muscular attachment) according to: fd = 2vf,cosplc,
Fig. 1. Diagram
of the ultrasound duplex-Doppler acquisition system.
image
(1)
where fd is the Doppler frequency shift, f0 is the frequency of the entrance ultrasound beam, c is the speed of sound in tissue (approximately 1540 m/s) and p is the angle between the ultrasound Doppler beam and the path of the moving object. It should be noted that objects moving in a direction perpendicular to the
Hyoid bone movementduring swallowing
Fig. 2. A standard mid-line sagittal ultrasound Doppler image of the tongue and hyomuscular region with a Doppler beam and sampling volume.
Doppler beam will be not detected because the angle p will be 90”, thus forcing fd to zero. Therefore, the ultrasound transducer was carefully adjusted during the swallowing studies to obtain Doppler spectral signals for the entire sequence of hyoid movement. There were several machine settings that were crucial to acquire clean and consistent Doppler spectra. A high-pass filter with a cutoff frequency of 50 Hz, described for clinical application as a “wall filter,” was used to eliminate spurious low-frequency Doppler shifts related to random fluctuations of the signal and a variety of motions from subcutaneous tissues of the floor of the mouth. These motions normally are < 50 Hz and, therefore, can be easily avoided using appropriate high-pass filtering. The 50-Hz wall filter (high pass) that we chose corresponds to cutting off slow
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The Doppler sampling volume is another parameter that affects the Doppler spectrum. Doppler signals are only obtained from nonperpendicular movement through the area of the sampling volume (Fig. 2). Doppler shift signals are generated when objects within the sampling volume move relative to the Doppler beam. It should be noted that when a swallow starts, the hyoid bone itself will not always remain in contact with the small sampling volume (2 or 3 mm). Using a larger sampling volume to cover the hyoid bone movement cannot provide a better solution for monitoring of the hyoid because more nonrelated Doppler shift signals and noise will be detected. Since the dynamics of the surrounding
muscular complex attached
to the hyoid bone are directly related to hyoid bone motion (i.e., the muscles move in synchrony with the bone to which they attach), it was valid to assume that the Doppler spectra reflected the motion of the hyoid bone, even in the special case when the hyoid bone itself had moved outside the sampling volume. System settings that affect the amplitude of the Doppler sig-
signals that are 5 0.7 cm/s, which is far less than our
nals, such as gain, were not important in our analysis, since we were only interested in the timing of swallow events. Ultrasound duplex-Doppler images were digitized using a Scion LG-3 frame grabber board on a Quadra 700 Macintosh computer. Figure 3 is a typical duplexDoppler image that includes simultaneous display of a 2D B-mode image and a Doppler spectrum. The hyoid bone muscular attachment, the acoustic shadow, the Doppler beam and sampling volume can be seen from the B-mode echographic image, which is shown
signals, which range up to 20 or 25 cm/set. Hence, the 50-Hz wall filter does not introduce inaccuracies. Nyquist’s theorem gives an upper limit to the measurable Doppler frequency, which must be lower than half the sampling frequency. When using ultrasound, the sampling frequency is known as the pulse repetition frequency (PRF), which is the number of acoustic pulses transmitted from the transducer per second (Hagen-Ansert 1989). Limiting Doppler signals to within this bound prevents aliasing, in which the Doppler frequencies above the Nyquist limit are either inverted or cut off at the peaks ( Hagen-Ansert 1989). To measure high velocities of the moving hyoid bone, one must use a high PRF; however, this still limits observation to the lower frequencies of the Fourier spectrum. Since we were using a high-pass filter to cut off low frequencies below 50 Hz, it was not important for us to use a low PRF to preserve them. Therefore, to obtain a high bandwidth of Doppler signals, we chose a PRF of 3.7 kHz, which was the highest sample frequency that did not substantially reduce the frame rate of the B-scan.
Fig. 3. Duplex-Doppler image of a normal swallow. Ultrasound B-mode in the upper left box is displayed simultaneously with the moving Doppler spectrum in the lower right corner (horizontal axis shows time and vertical axis shows velocity). A is the initiation of the first Doppler burst (hyoid begins to elevate). B is the beginning of the second burst (hyoid has elevated and begins to move anteriorly). C is the beginning of the third burst (where hyoid begins descent). D is the end of the third burst (hyoid region returns to rest at termination of the swallow).
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in the upper left corner. The Doppler spectrum, which consists of a sequence of bursts, shows the velocity distribution of hyoid bone movement during swallowing, which can be seen in the lower right comer, with time on the horizontal axis and velocity on the vertical axis. We measured the time intervals between A and B, B and C and C and D. A corresponds to initiation of hyoid motion, B indicates full elevation and beginning of anterior motion, C corresponds to maximum anterior displacement and beginning of return motion and D indicates completion of the return to original resting position of the HMR and the accompanying acoustic shadow region. From these measures, we were able to determine the durations for different swallowing phases (Table 1) . The total swallow duration was calculated by determining the total length of the Doppler spectrum, i.e., the interval from A to D. Hyoid bone trajectory was determined by tracking the motion of the hyoid bone muscular attachment region from the B-mode images. Because of the limited image resolution of B-mode images and the variations in swallowing, a subject was asked to swallow 15 consecutive lo-mL water boluses. The hyoid position during each swallow was plotted showing the pathway from A to D as shown in Fig. 4. A triangular trajectory model was used to fit the data from the 15 swallows, which enabled us to calculate the displacements during the three swallowing phases (A to B; B to C; and C to D). Dividing the displacement by the appropriate duration produced velocity of hyoid bone movement during each swallowing phase. In this study, we did not analyze the amplitude of the Doppler signal, as our focus was on the timing aspect of hyoid trajectories.
Volume
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9, 1996 8uporlor (mm)
Antwiw (mm) -10
-8
Fig. 4. Triangular model scatter plot of normal hyoid bone trajectory of data points of 15 consecutive swallows (with lo-mL water boluses) in a normal male subject.
A total of six normal volunteers (four men and two women) who had normal swallows and were familiar with the use of diagnostic ultrasound were selected to participate in this study. All subjects were instructed to swallow lo-mL water boluses while duplex-Doppler image data were acquired. Three male subjects (ages 43,63 and 76 y ) with swallowing disorders resulting from neuromuscular diseases were evaluated and their results compared to the normals. RESULTS
Table 1. Duration measurements (in s) of a normal, 30year-old, male subject (with IO-mL water boluses). Swallow 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Mean SD Max Min
Elevation (A-W 0.38 0.40 0.42 0.37 0.24 0.35 0.45 0.42 0.38 0.33 0.43 0.33 0.45 0.35 0.25 0.37 0.06 0.45 0.24
Anterior (B-C) 0.64 0.55 0.58 0.75 0.63 0.56 0.52 0.65 0.52 0.62 0.57 0.65 0.55 0.62 0.58 0.60 0.06 0.75 0.52
Return (C-D) 0.25 0.26 0.29 0.25 0.28 0.35 0.35 0.26 0.35 0.22 0.35 0.29 0.32 0.28 0.45 0.30 0.06 0.45 0.22
Total (A-D) 1.27 1.22 1.29 1.38 1.15 1.26 1.32 1.34 1.25 1.16 1.35 1.27 1.32 1.25 1.29 1.28 0.06 1.38 1.15
Normals Consistently similar Doppler shift patterns were found among all the normal subjects in the study. Figure 3 shows a typical Doppler shift pattern of a normal swallow with three distinct bursts of motion. A trajectory of the hyoid bone movement was obtained by tracking the hyoid bone muscular attachment region from the B-mode images. Figure 4 shows the trajectories of 15 swallows of one normal subject. It demonstrates that a normal swallow generally consists of three phases. First, the hyoid bone elevated from its resting position (A to B ) after a swallow was initiated. Second, the hyoid bone moved anteriorly to reach its maximum displacement (B to C). Finally, the hyoid bone returned to its resting position (C to D) . The Doppler spectral pattern from Fig. 3 displays these three phases as indicated by A to B, B to C and C to D. These phases are represented by the triangular trajectory model seen in Fig. 4.
Hyoid
bone movement
during
swatlowing
0 B. C. SONIES ef al.
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Table 2. Duration measurements (in s) of six normal subjects (with lo-mL water boluses). Subject #l (30M) 15 1.28 0.06 1.38 1.15
No. trials Mean SD Max Min
Subject
CUM)
#2
Subject #3 (19M)
Subject #4 (35M)
Subject #5 (32~)
Subject #6 (5OF)
12 1.30 0.04 I .36 I .25 -
IO 1.14 0.06 1.21 1.04
12 0.97 0.04 1.05 0.92
12 1.03 0.05 1.11 0.95
8 1.39 0.05 I .45 1.33
Table 1 shows the duration measurements of one normal subject (the subject whose swallow pattern is shown in Fig. 3) for 15 controlled swallows of 10 mL of water. The average durations of hyoid bone elevation, anterior movement and returning to rest were 0.37, 0.60 and 0.30 s, respectively. The average total swallow duration was 1.28 s (SD 0.06 s). Table 2 summarizes the duration measurements of all six normal subjects in our study. The total swallowing durations varied from 0.97 - 1.39 s, indicating individual differences among subjects. Despite these differences, the SDS within each subject were small (0.040.06 s) , showing minimal within-subject variability. We analyzed the trajectories of three of the six normals whose Doppler spectra were considered representative of the entire normal sample. Table 3 shows the swallowing durations and velocity measures of hyoid bone movement of the three normal subjects. The anterior hyoid movement (B-C) took longer than the other two phases, partially because of a pause that always occurred after the hyoid bone reached its maximum displacement. The distance traveled in the return movement of the hyoid bone (interval C-D) is the largest distance traveled by the hyoid bone in the swallow cycle. This fact and the short duration measurement for the C-D phase are responsible for the observation that the velocity of the hyoid bone is greatest during this portion of the swallow. Patients The three patients with swallowing disorders all presented patterns of hyoid motion that differed from
the patterns of the control subjects. Abnormalities were characterized by multiple swallows and hesitations. This pattern can be seen in Fig. 5 for a 43-year-old man swallowing a IO-mL water bolus. Two discrete swallows were produced (Al to D, and A2 to D2), with a pause in mid-sequence. The duration of 3.36 s was three times that of the control average. The trajectory of this swallow is plotted in Fig. 6. Here, we can see two almost identical sequences with their start (A, ) and completion (D,) located in a relatively close position. The start of the second swallow (A?) occurred with the hyoid bone held more superiorly and anteriorly than the first swallow, but followed a similar trajectory in a slightly more elevated plane. The same double swallow pattern (A, to DI and A, to D2) activity, with added pauses and irregular motion, can be seen in Figs. 7 (76-year-old man) and 8 (63-year-old man). DISCUSSION The ultrasound Doppler technique detects the motion of an object based on Doppler shift spectral analysis. An ultrasound beam of a fixed frequency reflects from the object, which generates a reflecting beam with a different frequency if there is relative movement between the entrance ultrasound beam and the object. In our study, the ultrasound Doppler spectrum reflected the movement pattern of the muscles surrounding the hyoid bone relative to the ultrasound beam. We achowledge that motion of the HMR that is perpendicular to the Doppler beam will be missed. Only a small portion of the trajectory would
Table 3. Duration (d) and velocity (v) measurements of three normal Subject
Mean SD Max Min d (mm) v (mm/s) d = distance
#l (30M)
Subject
subjects
(with lo-mL water bolus).
#2 (19M)
Subject
#3 (35M)
Elevation (A-B)
Anterior G-C)
Return (C-D)
Elevation (A-W
Anterior (B-C)
Return (C-D)
Elevation (A-B)
Anterior (B-C)
Return (C-D)
0.37 0.06 0.45 0.24 7.3 19.73
0.60 0.06 0.75 0.52 8.1 13.52
0.30 0.06 0.45 0.22 11.3 37.25
0.30 0.05 0.36 0.21 5.4 18.15
0.63 0.04 0.69 0.55 9.6 15.26
0.37 0.06 0.45 0.25 12.6 33.98
0.30 0.04 0.36 0.24 5.9 19.87
0.46 0.03 0.50 0.42 8.8 19.26
0.39 0.04 0.48 0.34 12.9 33.08
Ultrasound in MedicineandBiology
Volume22, Number9, 1996
Fig. 5. Doppler spectralpattern of swallows(lo-mL water bolus)of a 43-year-oldmalepatientwith polymyositis(horizontal axis showstime and vertical axis showsvelocity). Note that two swallow sequenceswere necessaryin this abnormalcase(seeFig. 6).
Fig. 7. Doppler spectralpattern of swallows( IO-mL.water bolus) of a 76-year-old male patient with inclusion body myositis(horizontal axis showstime andvertical axis shows velocity). Note that two completeswallowsare requiredin this abnormalcase.
be perpendicular at a given moment, thus reducing erroneous signals. Also, since we were primarily interested in the timing of hyoid movement, this missed data would not affect our overall results, which depend on the initiation and termination of movement (i.e., total swallow duration). We have determined that ultrasound duplex-Doppler imaging can be used to evaluate normal and abnormal hyoid bone movements during swallowing and is a useful tool to monitor swallowing pathologies. The three phases of a swallow determined by tracking hyoid bone motion
can be clearly differentiated on the Doppler spectrum. Our study has demonstrated the consistency of Doppler spectral patterns among normal subjects. Because the Doppler shift frequency of the hyoid muscular region is highly sensitive to movement, Doppler spectral analysis provides more accurate measurement of swallow duration than frame-by-frame analysis of x-ray videofluoroscopic images or conventional B-mode scans (Sonies et al. 1988). Doppler spectral analysis eliminates the subjective component in determining the start and end frames of a swallow in the frame-by-frame analysis procedure used in typical ultrasound B-mode swallow studies per-
Suporlor (mm)
Anterior (mm) I
-14
”
-12
-10
-0
-6
-4
-2
0
Fig. 6. Abnormal trajectory: Multiple swallowsare needed to clear a single lo-mL water bolus in the patient whose Doppler spectralpattern is shownin Fig. 5.
Fig. 8. Doppler spectralpattern of swallows(10-r& water bolus) of a 63-year-old male patient with inclusion body myositis(horizontal axis showstime andvertical axis shows velocity). Note the irregular activity in AI-D, and the second swallow sequencein this abnormalcase.
Hyoid bone movement during swallowing 0 B. C.
formed in our laboratory (Sonies et al. 1988; Sonies and Dalakas 1991). There are several factors that need monitoring when conducting Doppler studies. We found that, even when there was no swallow, we could obtain the Doppler shift signals by moving the ultrasound transducer rapidly across the chin, causing relative movements between the entrance ultrasound beam and the internal structures such as the hyoid bone. We therefore caution that motion of the ultrasound transducer must be minimized to achieve meaningful and consistent Doppler spectral patterns of hyoid bone movement. Additionally, several machine settings must be correctly selected when acquiring the Doppler spectra. An appropriately selected “wall filter” will be able to eliminate the spurious Doppler shift frequencies caused by movements of the muscles of the mouth and tongue. The PRF also needs to be carefully chosen to prevent aliasing within the Doppler spectrum. The Doppler and B-mode gains should be adjusted during duplex-Doppler acquisition to improve the qualities of both Doppler spectra and echographic images. CONCLUSIONS Ultrasound duplex-Doppler imaging and Doppler spectral analysis provide a new method for defining hyoid position and displaying accurate movement, which may be useful in the diagnosis of swallowing disorders. The duplex-Doppler imaging procedure provides clinically important information on hyoid bone velocity, trajectory and swallowing duration that can be used to differentiate normal from abnormal motion patterns. Similar results can be obtained on B-mode ultrasound and x-ray videofluoroscopy. However, ultrasound has a distinct advantage: there is no patient radiation exposure, which allows for repeated diagnostic studies. We will direct our future efforts toward studying the duplex-Doppler imaging technique on a larger patient pool. Because of these clinical advantages, we plan to evaluate the use of Doppler spectral analysis to differ-
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entiate hyoid bone movement patterns among other common conditions causing abnormal swallows. Acknowledgements-The authors appreciate the helpful discussions with Kenneth Kempner, M.S., from the Division of Computer Research and Technology at the NIH, and with Kenneth Watkin, Ph.D., from McGill University, Montreal, Canada.
REFERENCES Brown B. Sonies BC. Other dysphagia imaging procedures. In: Schulze K, Perman A, eds. Deglutition: Physiology, pathophysiology, diagnosis and management. San Diego: Singular Pub. Group, Inc., 1996:227-253. Cordaro MA, Sonies BC. An image processing scheme to quantitatively extract and validate hyoid bone motion based on real-time ultrasound recordings of swallowing. IEEE Trans Biomed Eng 1993;40:841-844. Davidson SL. Doppler auscultation an aid in temporomandibular joint diagnosis: J Craniomandibular Disorders 1988;2: 128- 132. Dodds WJ, Man KM, Cook IJ, et al. Influence of bolus volume on swallow-induced hyoid movement in normal subjects. Am J Radiol 1988;150:1307-1309. Ekberg 0. The normal movement of the hyoid bone during swallow. Invest Radio1 1986:21:408-410. Hagen-Ansert LS. Textbook of diagnostic ultrasonography, 3rd ed. St. Louis, MO: The C.V. Mosby Company, 1989. Marini M, Odoardi GL, Bolle G, Tartaglia P. Duplex-Doppler spectral analysis in the physiopathology of the temporomandibular joint. Computerized Med Imag Graph 1994; 18:35-43. Shawker TH, Sonies BC. Stone M, Baum BJ. Real-time ultrasound visualization of tongue movement during swallowing. Clin J Ultrasound 1983; 11:495-490. Shawker TH, Sonies BC, Hall TE, Baum BJ. Ultrasound analysis of tongue, hyoid and larynx activity during swallow. Invest Radio1 1984a; 19:82-86. Shawker TH, Sonies BC. Stone M. Soft tissue anatomy of the tongue and floor of the mouth: An ultrasound demonstration. Brain Lang 1984b;21:335-350. Sonies BC. Shawker TH. Hall TE, Gerber LH, Leighton SB. Ultrasonic visualization of tongue motion during speech. J Acoust Sot Am 1981;70:683-686. Sonies BC, Parent L, Morrish K, Baum BJ. Durational aspects of the oral-pharyngeal swallow in normal adults. Dysphagia 1988;3:637-648. Sonies BC, Dalakas M. Dysphagia in patients with postpolio syndrome: An overlooked phenomenon in polio survivors. N Engl J Med 1991:324:1162-1167. Sonies BC, Stone M. Speech imaging. In: McNeil M, ed. Clinical management of sensorimotor speech disorders. New York: Thieme Medical Publishers, 1996:177-191. Wintzen AR, Badrising UA, Roos RAC, Vielvoye J. Liauw L. Influence of bolus volume on hyoid movements in normal individuals and patients with Parkinson’s disease. Can J Neurol Sci 1994; 21~57-59.
Ultrasound
Copyright
PII: SO301-5629( 96)00158-S
ELSEVIER
l
Original Contribution EVALUATION OF NORMAL AND ABNORMAL HYOID BONE MOVEMENT DURING SWALLOWING BY USE OF ULTRASOUND DUPLEX-DOPPLER IMAGING BARBARA C. SONIES,+ CHENG WANG* and DARREN J. SAPPER’ +Rehabilitation Medicine Department, National Institutes of Health, Bethesda, MD: and ‘Allied Imaging International, Inc., Germantown, MD (Received
20 Fehruqv
1996; in finulforttz
I Augusf
1996)
Abstract-We developed a new method to analyze normal and abnormal movements of the hyoid muscular region as an indicator of hyoid bone motion during swallowing using ultrasound duplex-Doppler imaging. Hyoid bone motion can be monitored by studying the Doppler shift spectra and B-mode images produced by ultrasound duplex imaging of the hyoid region muscular attachments. We can accurately determine swallowing duration and trajectory of hyoid bone movement. This procedure can assist in discriminating between normal and abnormal movements of the hyoid bone and the surrounding muscles during swallowing. This method appears to be a highly consistent measure. We suggest that Doppler spectrum analysis can be used for defining hyoid position and displaying accurate movement, which may he useful in the Copyright 0 1996 World Federation for Ultrasound in Medicine & Biology diagnosis of swallowing disorders. Key Words: Ultrasound
imaging, Ultrasound
duplex-Doppler
INTRODUCTION
radiology. Being able to provide real-time images, ultrasound imaging techniques have been used in speech and swallowing studies (Cordaro and Sonies 1993; Shawker et al. 1983, 1984a; Sonies et al. 1981, 1988) and in the study of soft tissue anatomy of the tongue and floor of the mouth (Shawker et al. 1984b). Although ultrasound cannot display the hyoid bone itself, conventional Bmode scanning can still be used to monitor hyoid bone movement by analyzing the motion of its acoustic shadow and the surrounding muscle tissues (i.e., the hyomuscular attachment region) (Brown and Sonies 1996; Sonies and Stone 1996). The ultrasonic duplex-Doppler imaging technique, which provides both echographic B-mode images and Doppler shift spectra, is frequently used to analyze motion of blood flow through the cardiovascular system. Davidson (1988) used Doppler methods along with other velocimetric techniques to study the temporomandibular joint (TMJ) Marini et al. ( 1994) reported a novel approach to evaluate the pathophysiology of the TMJ by using ultrasound duplex-Doppler spectral analysis techniques. In their study, joint movement was analyzed by computing the Fourier transform of the time signals. which gave the velocity distribution of the condylo-mensical complex during opening and closing of the jaw. They were able to discriminate
The larynx and pharynx are muscular tubes surrounded by a suspensory system composed of the hyoid bone and the thyroid and cricoid cartilages, which are all interlinked by ligaments and tendons. These structures maintain the lumen of the pharynx and larynx. The whole complex is attached to the base of the skull, mandible, spine and thoracic skeleton. The supra- and infrahyoid muscles (mylohyoid, geniohyoid, digastic, stylohyoid) all attach to the hyoid bone beneath the chin in a submental position. This area can be called the hyomuscular region (HMR). The hyoid bone, which has a characteristic radiographic appearance, is a critical component of this system. The movement of the hyoid bone is thought to be important for closure of the airway, including the lowering of the epiglottis and the adduction of the vocal folds. Movement of the hyoid bone is traditionally studied using x-ray fluoroscopy, which exposes subjects to radiation (Dodds et al. 1988; Ekberg 1986; Wintzen et al. 1994). However, as a noninvasive technology, ultrasound imaging is playing a growing role in diagnostic Address correspondence Speech-Language Pathology partment, National Institutes
imaging, Hyoid bone motion, Swallowing.
to: Dr. Barbara C. Sonies, Chief. Section, Rehabilitation Medicine Deof Health, Bethesda, MD 20892. 1169
1170
Ultrasound in Medicine and Biology
between normal and abnormal motions of the condylomensical complex. We propose the use of ultrasound duplex-Doppler imaging for the assessment of hyoid bone motion during swallowing. To investigate the feasibility of using ultrasound duplex-Doppler imaging for assessing the movement of the hyoid bone during swallowing, we have developed a computerized image acquisition and processing system that allows us to acquire B-mode ultrasound images and analyze Doppler spectra data. Using our technique, we studied controlled water bolus swallows of normal subjects and patients with swallowing disorders. We compared swallow duration, hyoid bone movement trajectories and hyoid bone velocities based upon the displacement of the HMR to evaluate swallowing. We describe the image acquisition and processing system and the results of the analysis of normal and abnormal hyoid bone movement. MATERIALS
AND METHODS
An ATL Ultramark 9 HDI ultrasound scanner (Advanced Technology Laboratories, Inc., Bothell, WA, USA) was used for the studies. Images were acquired using a curved array transducer with an operating frequency range from 5.0-9.0 MHz and a Doppler frequency of 5.0 MHz. Figure 1 shows a configuration diagram of our ultrasound duplex-Doppler
n $ Subject
Ultrasound Transducer
ATL Ultramark 9 Ultrasound Imaging
Volume 22, Number 9, 1996
image acquisition system. To obtain images, the transducer was placed submentally under the subject’s chin and angled back toward the hyoid bone shadow, with the hyomuscular attachment region in clear view. The position and orientation of the transducer and the position of the sampling volume were adjusted by viewing the two-dimensional (2D) echographic images. The images containing both the 2D images and Doppler spectra were recorded on video tape for analysis. A time code indicating the video frame was inserted on the images (Horita TRG-50, Horita, Mission Viejo, CA, USA). The image data on the tape were digitized using a frame grabber board (Scion LG-3, Scion Corporation, Frederick, MD, USA) on a Macintosh Quadra 700 computer (Apple Computer, Inc., Santa Clara, CA, USA). Two dimensional B-mode echographic images were displayed simultaneously with Doppler spectral signals. Simultaneous display was needed to adjust the size and position of the Doppler sampling volume as well as to adjust the angle between the ultrasound beam and the hyoid bone. The hyomuscular attachment region, where all the muscles attach to the superior cornu of the hyoid bone, creates a highly echoic region in the image. The sample volume is positioned over this readily visible region. The acoustic shadow of the hyoid is an echo-free triangular area adjacent to the HMR through which the Doppler beam passes (Fig. 2). Figure 2 shows a standard mid-line sagittal ultrasound Doppler image through the tongue and oral cavity, with the central axis of the Doppler beam and fixed sampling volume indicated. On the B-mode image, the Doppler beam was oriented through the HMR, which could be seen as a bright area (boxed in) at the origin of the acoustic shadow cast by the hyoid bone. Because ultrasound does not image bone, this technique relies upon measuring the displacement motion through the fixed sample volume of the HMR. The ATL Doppler equipment is designed to display the beam’s central axis and selected sample volume. The initial motion of the HMR away from the transducer produces a Doppler frequency shift. The Doppler frequency shift depends on the velocity, u, of the observed object (i.e. , the hyoid bone and its surrounding muscular attachment) according to: fd = 2vf,cosplc,
Fig. 1. Diagram
of the ultrasound duplex-Doppler acquisition system.
image
(1)
where fd is the Doppler frequency shift, f0 is the frequency of the entrance ultrasound beam, c is the speed of sound in tissue (approximately 1540 m/s) and p is the angle between the ultrasound Doppler beam and the path of the moving object. It should be noted that objects moving in a direction perpendicular to the
Hyoid bone movementduring swallowing
Fig. 2. A standard mid-line sagittal ultrasound Doppler image of the tongue and hyomuscular region with a Doppler beam and sampling volume.
Doppler beam will be not detected because the angle p will be 90”, thus forcing fd to zero. Therefore, the ultrasound transducer was carefully adjusted during the swallowing studies to obtain Doppler spectral signals for the entire sequence of hyoid movement. There were several machine settings that were crucial to acquire clean and consistent Doppler spectra. A high-pass filter with a cutoff frequency of 50 Hz, described for clinical application as a “wall filter,” was used to eliminate spurious low-frequency Doppler shifts related to random fluctuations of the signal and a variety of motions from subcutaneous tissues of the floor of the mouth. These motions normally are < 50 Hz and, therefore, can be easily avoided using appropriate high-pass filtering. The 50-Hz wall filter (high pass) that we chose corresponds to cutting off slow
l
B. C.
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The Doppler sampling volume is another parameter that affects the Doppler spectrum. Doppler signals are only obtained from nonperpendicular movement through the area of the sampling volume (Fig. 2). Doppler shift signals are generated when objects within the sampling volume move relative to the Doppler beam. It should be noted that when a swallow starts, the hyoid bone itself will not always remain in contact with the small sampling volume (2 or 3 mm). Using a larger sampling volume to cover the hyoid bone movement cannot provide a better solution for monitoring of the hyoid because more nonrelated Doppler shift signals and noise will be detected. Since the dynamics of the surrounding
muscular complex attached
to the hyoid bone are directly related to hyoid bone motion (i.e., the muscles move in synchrony with the bone to which they attach), it was valid to assume that the Doppler spectra reflected the motion of the hyoid bone, even in the special case when the hyoid bone itself had moved outside the sampling volume. System settings that affect the amplitude of the Doppler sig-
signals that are 5 0.7 cm/s, which is far less than our
nals, such as gain, were not important in our analysis, since we were only interested in the timing of swallow events. Ultrasound duplex-Doppler images were digitized using a Scion LG-3 frame grabber board on a Quadra 700 Macintosh computer. Figure 3 is a typical duplexDoppler image that includes simultaneous display of a 2D B-mode image and a Doppler spectrum. The hyoid bone muscular attachment, the acoustic shadow, the Doppler beam and sampling volume can be seen from the B-mode echographic image, which is shown
signals, which range up to 20 or 25 cm/set. Hence, the 50-Hz wall filter does not introduce inaccuracies. Nyquist’s theorem gives an upper limit to the measurable Doppler frequency, which must be lower than half the sampling frequency. When using ultrasound, the sampling frequency is known as the pulse repetition frequency (PRF), which is the number of acoustic pulses transmitted from the transducer per second (Hagen-Ansert 1989). Limiting Doppler signals to within this bound prevents aliasing, in which the Doppler frequencies above the Nyquist limit are either inverted or cut off at the peaks ( Hagen-Ansert 1989). To measure high velocities of the moving hyoid bone, one must use a high PRF; however, this still limits observation to the lower frequencies of the Fourier spectrum. Since we were using a high-pass filter to cut off low frequencies below 50 Hz, it was not important for us to use a low PRF to preserve them. Therefore, to obtain a high bandwidth of Doppler signals, we chose a PRF of 3.7 kHz, which was the highest sample frequency that did not substantially reduce the frame rate of the B-scan.
Fig. 3. Duplex-Doppler image of a normal swallow. Ultrasound B-mode in the upper left box is displayed simultaneously with the moving Doppler spectrum in the lower right corner (horizontal axis shows time and vertical axis shows velocity). A is the initiation of the first Doppler burst (hyoid begins to elevate). B is the beginning of the second burst (hyoid has elevated and begins to move anteriorly). C is the beginning of the third burst (where hyoid begins descent). D is the end of the third burst (hyoid region returns to rest at termination of the swallow).
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in the upper left corner. The Doppler spectrum, which consists of a sequence of bursts, shows the velocity distribution of hyoid bone movement during swallowing, which can be seen in the lower right comer, with time on the horizontal axis and velocity on the vertical axis. We measured the time intervals between A and B, B and C and C and D. A corresponds to initiation of hyoid motion, B indicates full elevation and beginning of anterior motion, C corresponds to maximum anterior displacement and beginning of return motion and D indicates completion of the return to original resting position of the HMR and the accompanying acoustic shadow region. From these measures, we were able to determine the durations for different swallowing phases (Table 1) . The total swallow duration was calculated by determining the total length of the Doppler spectrum, i.e., the interval from A to D. Hyoid bone trajectory was determined by tracking the motion of the hyoid bone muscular attachment region from the B-mode images. Because of the limited image resolution of B-mode images and the variations in swallowing, a subject was asked to swallow 15 consecutive lo-mL water boluses. The hyoid position during each swallow was plotted showing the pathway from A to D as shown in Fig. 4. A triangular trajectory model was used to fit the data from the 15 swallows, which enabled us to calculate the displacements during the three swallowing phases (A to B; B to C; and C to D). Dividing the displacement by the appropriate duration produced velocity of hyoid bone movement during each swallowing phase. In this study, we did not analyze the amplitude of the Doppler signal, as our focus was on the timing aspect of hyoid trajectories.
Volume
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9, 1996 8uporlor (mm)
Antwiw (mm) -10
-8
Fig. 4. Triangular model scatter plot of normal hyoid bone trajectory of data points of 15 consecutive swallows (with lo-mL water boluses) in a normal male subject.
A total of six normal volunteers (four men and two women) who had normal swallows and were familiar with the use of diagnostic ultrasound were selected to participate in this study. All subjects were instructed to swallow lo-mL water boluses while duplex-Doppler image data were acquired. Three male subjects (ages 43,63 and 76 y ) with swallowing disorders resulting from neuromuscular diseases were evaluated and their results compared to the normals. RESULTS
Table 1. Duration measurements (in s) of a normal, 30year-old, male subject (with IO-mL water boluses). Swallow 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Mean SD Max Min
Elevation (A-W 0.38 0.40 0.42 0.37 0.24 0.35 0.45 0.42 0.38 0.33 0.43 0.33 0.45 0.35 0.25 0.37 0.06 0.45 0.24
Anterior (B-C) 0.64 0.55 0.58 0.75 0.63 0.56 0.52 0.65 0.52 0.62 0.57 0.65 0.55 0.62 0.58 0.60 0.06 0.75 0.52
Return (C-D) 0.25 0.26 0.29 0.25 0.28 0.35 0.35 0.26 0.35 0.22 0.35 0.29 0.32 0.28 0.45 0.30 0.06 0.45 0.22
Total (A-D) 1.27 1.22 1.29 1.38 1.15 1.26 1.32 1.34 1.25 1.16 1.35 1.27 1.32 1.25 1.29 1.28 0.06 1.38 1.15
Normals Consistently similar Doppler shift patterns were found among all the normal subjects in the study. Figure 3 shows a typical Doppler shift pattern of a normal swallow with three distinct bursts of motion. A trajectory of the hyoid bone movement was obtained by tracking the hyoid bone muscular attachment region from the B-mode images. Figure 4 shows the trajectories of 15 swallows of one normal subject. It demonstrates that a normal swallow generally consists of three phases. First, the hyoid bone elevated from its resting position (A to B ) after a swallow was initiated. Second, the hyoid bone moved anteriorly to reach its maximum displacement (B to C). Finally, the hyoid bone returned to its resting position (C to D) . The Doppler spectral pattern from Fig. 3 displays these three phases as indicated by A to B, B to C and C to D. These phases are represented by the triangular trajectory model seen in Fig. 4.
Hyoid
bone movement
during
swatlowing
0 B. C. SONIES ef al.
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Table 2. Duration measurements (in s) of six normal subjects (with lo-mL water boluses). Subject #l (30M) 15 1.28 0.06 1.38 1.15
No. trials Mean SD Max Min
Subject
CUM)
#2
Subject #3 (19M)
Subject #4 (35M)
Subject #5 (32~)
Subject #6 (5OF)
12 1.30 0.04 I .36 I .25 -
IO 1.14 0.06 1.21 1.04
12 0.97 0.04 1.05 0.92
12 1.03 0.05 1.11 0.95
8 1.39 0.05 I .45 1.33
Table 1 shows the duration measurements of one normal subject (the subject whose swallow pattern is shown in Fig. 3) for 15 controlled swallows of 10 mL of water. The average durations of hyoid bone elevation, anterior movement and returning to rest were 0.37, 0.60 and 0.30 s, respectively. The average total swallow duration was 1.28 s (SD 0.06 s). Table 2 summarizes the duration measurements of all six normal subjects in our study. The total swallowing durations varied from 0.97 - 1.39 s, indicating individual differences among subjects. Despite these differences, the SDS within each subject were small (0.040.06 s) , showing minimal within-subject variability. We analyzed the trajectories of three of the six normals whose Doppler spectra were considered representative of the entire normal sample. Table 3 shows the swallowing durations and velocity measures of hyoid bone movement of the three normal subjects. The anterior hyoid movement (B-C) took longer than the other two phases, partially because of a pause that always occurred after the hyoid bone reached its maximum displacement. The distance traveled in the return movement of the hyoid bone (interval C-D) is the largest distance traveled by the hyoid bone in the swallow cycle. This fact and the short duration measurement for the C-D phase are responsible for the observation that the velocity of the hyoid bone is greatest during this portion of the swallow. Patients The three patients with swallowing disorders all presented patterns of hyoid motion that differed from
the patterns of the control subjects. Abnormalities were characterized by multiple swallows and hesitations. This pattern can be seen in Fig. 5 for a 43-year-old man swallowing a IO-mL water bolus. Two discrete swallows were produced (Al to D, and A2 to D2), with a pause in mid-sequence. The duration of 3.36 s was three times that of the control average. The trajectory of this swallow is plotted in Fig. 6. Here, we can see two almost identical sequences with their start (A, ) and completion (D,) located in a relatively close position. The start of the second swallow (A?) occurred with the hyoid bone held more superiorly and anteriorly than the first swallow, but followed a similar trajectory in a slightly more elevated plane. The same double swallow pattern (A, to DI and A, to D2) activity, with added pauses and irregular motion, can be seen in Figs. 7 (76-year-old man) and 8 (63-year-old man). DISCUSSION The ultrasound Doppler technique detects the motion of an object based on Doppler shift spectral analysis. An ultrasound beam of a fixed frequency reflects from the object, which generates a reflecting beam with a different frequency if there is relative movement between the entrance ultrasound beam and the object. In our study, the ultrasound Doppler spectrum reflected the movement pattern of the muscles surrounding the hyoid bone relative to the ultrasound beam. We achowledge that motion of the HMR that is perpendicular to the Doppler beam will be missed. Only a small portion of the trajectory would
Table 3. Duration (d) and velocity (v) measurements of three normal Subject
Mean SD Max Min d (mm) v (mm/s) d = distance
#l (30M)
Subject
subjects
(with lo-mL water bolus).
#2 (19M)
Subject
#3 (35M)
Elevation (A-B)
Anterior G-C)
Return (C-D)
Elevation (A-W
Anterior (B-C)
Return (C-D)
Elevation (A-B)
Anterior (B-C)
Return (C-D)
0.37 0.06 0.45 0.24 7.3 19.73
0.60 0.06 0.75 0.52 8.1 13.52
0.30 0.06 0.45 0.22 11.3 37.25
0.30 0.05 0.36 0.21 5.4 18.15
0.63 0.04 0.69 0.55 9.6 15.26
0.37 0.06 0.45 0.25 12.6 33.98
0.30 0.04 0.36 0.24 5.9 19.87
0.46 0.03 0.50 0.42 8.8 19.26
0.39 0.04 0.48 0.34 12.9 33.08
Ultrasound in MedicineandBiology
Volume22, Number9, 1996
Fig. 5. Doppler spectralpattern of swallows(lo-mL water bolus)of a 43-year-oldmalepatientwith polymyositis(horizontal axis showstime and vertical axis showsvelocity). Note that two swallow sequenceswere necessaryin this abnormalcase(seeFig. 6).
Fig. 7. Doppler spectralpattern of swallows( IO-mL.water bolus) of a 76-year-old male patient with inclusion body myositis(horizontal axis showstime andvertical axis shows velocity). Note that two completeswallowsare requiredin this abnormalcase.
be perpendicular at a given moment, thus reducing erroneous signals. Also, since we were primarily interested in the timing of hyoid movement, this missed data would not affect our overall results, which depend on the initiation and termination of movement (i.e., total swallow duration). We have determined that ultrasound duplex-Doppler imaging can be used to evaluate normal and abnormal hyoid bone movements during swallowing and is a useful tool to monitor swallowing pathologies. The three phases of a swallow determined by tracking hyoid bone motion
can be clearly differentiated on the Doppler spectrum. Our study has demonstrated the consistency of Doppler spectral patterns among normal subjects. Because the Doppler shift frequency of the hyoid muscular region is highly sensitive to movement, Doppler spectral analysis provides more accurate measurement of swallow duration than frame-by-frame analysis of x-ray videofluoroscopic images or conventional B-mode scans (Sonies et al. 1988). Doppler spectral analysis eliminates the subjective component in determining the start and end frames of a swallow in the frame-by-frame analysis procedure used in typical ultrasound B-mode swallow studies per-
Suporlor (mm)
Anterior (mm) I
-14
”
-12
-10
-0
-6
-4
-2
0
Fig. 6. Abnormal trajectory: Multiple swallowsare needed to clear a single lo-mL water bolus in the patient whose Doppler spectralpattern is shownin Fig. 5.
Fig. 8. Doppler spectralpattern of swallows(10-r& water bolus) of a 63-year-old male patient with inclusion body myositis(horizontal axis showstime andvertical axis shows velocity). Note the irregular activity in AI-D, and the second swallow sequencein this abnormalcase.
Hyoid bone movement during swallowing 0 B. C.
formed in our laboratory (Sonies et al. 1988; Sonies and Dalakas 1991). There are several factors that need monitoring when conducting Doppler studies. We found that, even when there was no swallow, we could obtain the Doppler shift signals by moving the ultrasound transducer rapidly across the chin, causing relative movements between the entrance ultrasound beam and the internal structures such as the hyoid bone. We therefore caution that motion of the ultrasound transducer must be minimized to achieve meaningful and consistent Doppler spectral patterns of hyoid bone movement. Additionally, several machine settings must be correctly selected when acquiring the Doppler spectra. An appropriately selected “wall filter” will be able to eliminate the spurious Doppler shift frequencies caused by movements of the muscles of the mouth and tongue. The PRF also needs to be carefully chosen to prevent aliasing within the Doppler spectrum. The Doppler and B-mode gains should be adjusted during duplex-Doppler acquisition to improve the qualities of both Doppler spectra and echographic images. CONCLUSIONS Ultrasound duplex-Doppler imaging and Doppler spectral analysis provide a new method for defining hyoid position and displaying accurate movement, which may be useful in the diagnosis of swallowing disorders. The duplex-Doppler imaging procedure provides clinically important information on hyoid bone velocity, trajectory and swallowing duration that can be used to differentiate normal from abnormal motion patterns. Similar results can be obtained on B-mode ultrasound and x-ray videofluoroscopy. However, ultrasound has a distinct advantage: there is no patient radiation exposure, which allows for repeated diagnostic studies. We will direct our future efforts toward studying the duplex-Doppler imaging technique on a larger patient pool. Because of these clinical advantages, we plan to evaluate the use of Doppler spectral analysis to differ-
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entiate hyoid bone movement patterns among other common conditions causing abnormal swallows. Acknowledgements-The authors appreciate the helpful discussions with Kenneth Kempner, M.S., from the Division of Computer Research and Technology at the NIH, and with Kenneth Watkin, Ph.D., from McGill University, Montreal, Canada.
REFERENCES Brown B. Sonies BC. Other dysphagia imaging procedures. In: Schulze K, Perman A, eds. Deglutition: Physiology, pathophysiology, diagnosis and management. San Diego: Singular Pub. Group, Inc., 1996:227-253. Cordaro MA, Sonies BC. An image processing scheme to quantitatively extract and validate hyoid bone motion based on real-time ultrasound recordings of swallowing. IEEE Trans Biomed Eng 1993;40:841-844. Davidson SL. Doppler auscultation an aid in temporomandibular joint diagnosis: J Craniomandibular Disorders 1988;2: 128- 132. Dodds WJ, Man KM, Cook IJ, et al. Influence of bolus volume on swallow-induced hyoid movement in normal subjects. Am J Radiol 1988;150:1307-1309. Ekberg 0. The normal movement of the hyoid bone during swallow. Invest Radio1 1986:21:408-410. Hagen-Ansert LS. Textbook of diagnostic ultrasonography, 3rd ed. St. Louis, MO: The C.V. Mosby Company, 1989. Marini M, Odoardi GL, Bolle G, Tartaglia P. Duplex-Doppler spectral analysis in the physiopathology of the temporomandibular joint. Computerized Med Imag Graph 1994; 18:35-43. Shawker TH, Sonies BC. Stone M, Baum BJ. Real-time ultrasound visualization of tongue movement during swallowing. Clin J Ultrasound 1983; 11:495-490. Shawker TH, Sonies BC, Hall TE, Baum BJ. Ultrasound analysis of tongue, hyoid and larynx activity during swallow. Invest Radio1 1984a; 19:82-86. Shawker TH, Sonies BC. Stone M. Soft tissue anatomy of the tongue and floor of the mouth: An ultrasound demonstration. Brain Lang 1984b;21:335-350. Sonies BC. Shawker TH. Hall TE, Gerber LH, Leighton SB. Ultrasonic visualization of tongue motion during speech. J Acoust Sot Am 1981;70:683-686. Sonies BC, Parent L, Morrish K, Baum BJ. Durational aspects of the oral-pharyngeal swallow in normal adults. Dysphagia 1988;3:637-648. Sonies BC, Dalakas M. Dysphagia in patients with postpolio syndrome: An overlooked phenomenon in polio survivors. N Engl J Med 1991:324:1162-1167. Sonies BC, Stone M. Speech imaging. In: McNeil M, ed. Clinical management of sensorimotor speech disorders. New York: Thieme Medical Publishers, 1996:177-191. Wintzen AR, Badrising UA, Roos RAC, Vielvoye J. Liauw L. Influence of bolus volume on hyoid movements in normal individuals and patients with Parkinson’s disease. Can J Neurol Sci 1994; 21~57-59.